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Disrupted cortical network as a vulnerability marker for obsessive–compulsive disorder

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Abstract

Morphological alterations of brain structure are generally assumed to be involved in the pathophysiology of obsessive–compulsive disorder (OCD). Yet, little is known about the morphological connectivity properties of structural brain networks in OCD or about the heritability of those morphological connectivity properties. To better understand these properties, we conducted a study that defined three different groups: OCD group with 30 subjects, siblings group with 19 subjects, and matched controls group with 30 subjects. A structural brain network was constructed using 68 cortical regions of each subject within their respective group (i.e., one brain network for each group). Both small-worldness and modularity were measured to reflect the morphological connectivity properties of each constructed structural brain network. When compared to the matched controls, the structural brain networks of patients with OCD indeed exhibited atypical small-worldness and modularity. Specifically, small-worldness showed decreased local efficiency, and modularity showed reduced intra-connectivity in Module III (default mode network) and increased interconnectivity between Module I (executive function) and Module II (cognitive control/spatial). Intriguingly, the structured brain networks of the unaffected siblings showed similar small-worldness and modularity as OCD patients. Based on the atypical structural brain networks observed in OCD patients and their unaffected siblings, abnormal small-worldness and modularity may indicate a candidate endophenotype for OCD.

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References

  • Achard S, Bullmore E (2007) Efficiency and cost of economical brain functional networks. PLoS Comput Biol 3:174–183

    Article  CAS  Google Scholar 

  • Ahmari SE, Risbrough VB, Geyer MA, Simpson HB (2012) Impaired sensorimotor gating in unmedicated adults with obsessive-compulsive disorder. Neuropsychopharmacology 37:1216–1223

    Article  PubMed Central  PubMed  Google Scholar 

  • Bassett DS, Bullmore E, Verchinski BA, Mattay VS, Weinberger DR, Meyer-Lindenberg A (2008) Hierarchical organization of human cortical networks in health and schizophrenia. J Neurosci 28:9239–9248

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Beck AT, Steer RA (1984) Internal consistencies of the original and revised Beck Depression Inventory. J Clin Psychol 40:1365–1367

    Article  CAS  PubMed  Google Scholar 

  • Biswal BB, Mennes M, Zuo XN, Gohel S, Kelly C, Smith SM, Beckmann CF, Adelstein JS, Buckner RL, Colcombe S, Dogonowski AM, Ernst M, Fair D, Hampson M, Hoptman MJ, Hyde JS, Kiviniemi VJ, Kotter R, Li SJ, Lin CP, Lowe MJ, Mackay C, Madden DJ, Madsen KH, Margulies DS, Mayberg HS, McMahon K, Monk CS, Mostofsky SH, Nagel BJ, Pekar JJ, Peltier SJ, Petersen SE, Riedl V, Rombouts SA, Rypma B, Schlaggar BL, Schmidt S, Seidler RD, Siegle GJ, Sorg C, Teng GJ, Veijola J, Villringer A, Walter M, Wang L, Weng XC, Whitfield-Gabrieli S, Williamson P, Windischberger C, Zang YF, Zhang HY, Castellanos FX, Milham MP (2010) Toward discovery science of human brain function. Proc Natl Acad Sci USA 107:4734–4739

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bullmore E, Sporns O (2009) Complex brain networks: graph theoretical analysis of structural and functional systems. Nat Rev Neurosci 10:186–198

    Article  CAS  PubMed  Google Scholar 

  • Bullmore ET, Suckling J, Overmeyer S, Rabe-Hesketh S, Taylor E, Brammer MJ (1999) Global, voxel, and cluster tests, by theory and permutation, for a difference between two groups of structural MR images of the brain. IEEE Trans Med Imaging 18:32–42

    Article  CAS  PubMed  Google Scholar 

  • Cavedini P, Zorzi C, Piccinni M, Cavallini MC, Bellodi L (2010) Executive dysfunctions in obsessive-compulsive patients and unaffected relatives: searching for a new intermediate phenotype. Biol Psychiatry 67:1178–1184

    Article  PubMed  Google Scholar 

  • Chamberlain SR, Fineberg NA, Menzies LA, Blackwell AD, Bullmore ET, Robbins TW, Sahakian BJ (2007) Impaired cognitive flexibility and motor inhibition in unaffected first-degree relatives of patients with obsessive-compulsive disorder. Am J Psychiatry 164:335–338

    Article  PubMed Central  PubMed  Google Scholar 

  • Chen ZJ, He Y, Rosa-Neto P, Germann J, Evans AC (2008) Revealing modular architecture of human brain structural networks by using cortical thickness from MRI. Cereb Cortex 18:2374–2381

    Article  PubMed Central  PubMed  Google Scholar 

  • Chen ZJ, He Y, Rosa-Neto P, Gong G, Evans AC (2011) Age-related alterations in the modular organization of structural cortical network by using cortical thickness from MRI. NeuroImage 56:235–245

    Article  PubMed  Google Scholar 

  • Christoff K, Gordon AM, Smallwood J, Smith R, Schooler JW (2009) Experience sampling during fMRI reveals default network and executive system contributions to mind wandering. Proc Natl Acad Sci USA 106:8719–8724

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Cocchi L, Harrison BJ, Pujol J, Harding IH, Fornito A, Pantelis C, Yucel M (2012) Functional alterations of large-scale brain networks related to cognitive control in obsessive-compulsive disorder. Hum Brain Mapp 33:1089–1106

    Article  PubMed  Google Scholar 

  • Desikan RS, Segonne F, Fischl B, Quinn BT, Dickerson BC, Blacker D, Buckner RL, Dale AM, Maguire RP, Hyman BT, Albert MS, Killiany RJ (2006) An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage 31:968–980

    Article  PubMed  Google Scholar 

  • Fan Q, Palaniyappan L, Tan L, Wang J, Wang X, Li C, Zhang T, Jiang K, Xiao Z, Liddle PF (2012) Surface anatomical profile of the cerebral cortex in obsessive-compulsive disorder: a study of cortical thickness, folding and surface area. Psychol Med 1–11

  • Ferrarini L, Veer IM, Baerends E, van Tol MJ, Renken RJ, van der Wee NJ, Veltman DJ, Aleman A, Zitman FG, Penninx BW, van Buchem MA, Reiber JH, Rombouts SA, Milles J (2009) Hierarchical functional modularity in the resting-state human brain. Hum Brain Mapp 30:2220–2231

    Article  PubMed  Google Scholar 

  • First MB SR, Williams JBW, Gibbon M. (1996) Structured Clinical Interview for DSM-IV (SCID). APA Press

  • First MB, Spitzer RL, Gibbon M, Williams JB (2002) Structured Clinical Interview for DSM-IV-TR Axis I Disorders, Research Version, Non-Patient Edition (SCID-I/NP). Biometrics Research Department, New York State Psychiatric Institute, New York

    Google Scholar 

  • Fischl B, Sereno MI, Dale AM (1999) Cortical surface-based analysis. II: inflation, flattening, and a surface-based coordinate system. Neuroimage 9:195–207

    Article  CAS  PubMed  Google Scholar 

  • Fitzgerald KD, Stern ER, Angstadt M, Nicholson-Muth KC, Maynor MR, Welsh RC, Hanna GL, Taylor SF (2010) Altered function and connectivity of the medial frontal cortex in pediatric obsessive-compulsive disorder. Biol Psychiatry 68:1039–1047

    Article  PubMed Central  PubMed  Google Scholar 

  • Foa EB, Huppert JD, Leiberg S, Langner R, Kichic R, Hajcak G, Salkovskis PM (2002) The Obsessive-Compulsive Inventory: development and validation of a short version. Psychol Assess 14:485–496

    Article  PubMed  Google Scholar 

  • Fortunato S, Barthelemy M (2007) Resolution limit in community detection. Proc Natl Acad Sci USA 104:36–41

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Gong YX (1992) Manual of Wechsler Adult Intelligence Scale: Chinese version. Chinese Map Press, Changsha

    Google Scholar 

  • Goodman WK, Price LH, Rasmussen SA, Mazure C, Fleischmann RL, Hill CL, Heninger GR, Charney DS (1989) The Yale-Brown Obsessive Compulsive Scale. I. Development, use, and reliability. Arch Gen Psychiatry 46:1006–1011

    Article  CAS  PubMed  Google Scholar 

  • Gusnard DA, Akbudak E, Shulman GL, Raichle ME (2001) Medial prefrontal cortex and self-referential mental activity: relation to a default mode of brain function. Proc Natl Acad Sci USA 98:4259–4264

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hagmann P, Cammoun L, Gigandet X, Meuli R, Honey CJ, Wedeen VJ, Sporns O (2008) Mapping the structural core of human cerebral cortex. PLoS Biol 6:e159

    Article  PubMed Central  PubMed  Google Scholar 

  • Harrison BJ, Pujol J, Lopez-Sola M, Hernandez-Ribas R, Deus J, Ortiz H, Soriano-Mas C, Yucel M, Pantelis C, Cardoner N (2008) Consistency and functional specialization in the default mode brain network. Proc Natl Acad Sci USA 105:9781–9786

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Harrison BJ, Soriano-Mas C, Pujol J, Ortiz H, Lopez-Sola M, Hernandez-Ribas R, Deus J, Alonso P, Yucel M, Pantelis C, Menchon JM, Cardoner N (2009) Altered corticostriatal functional connectivity in obsessive-compulsive disorder. Arch Gen Psychiatry 66:1189–1200

    Article  PubMed  Google Scholar 

  • He Y, Chen ZJ, Evans AC (2007) Small-world anatomical networks in the human brain revealed by cortical thickness from MRI. Cereb Cortex 17:2407–2419

    Article  PubMed  Google Scholar 

  • He Y, Chen Z, Evans A (2008) Structural insights into aberrant topological patterns of large-scale cortical networks in Alzheimer’s Disease. J Neurosci 28:4756–4766

    Article  CAS  PubMed  Google Scholar 

  • He Y, Dagher A, Chen Z, Charil A, Zijdenbos A, Worsley K, Evans A (2009) Impaired small-world efficiency in structural cortical networks in multiple sclerosis associated with white matter lesion load. Brain 132:3366–3379

    Article  PubMed Central  PubMed  Google Scholar 

  • Kocak OM, Ozpolat AY, Atbasoglu C, Cicek M (2011) Cognitive control of a simple mental image in patients with obsessive–compulsive disorder. Brain Cogn 76:390–399

    Article  PubMed  Google Scholar 

  • Kuhn S, Kaufmann C, Simon D, Endrass T, Gallinat J, Kathmann N (2012) Reduced thickness of anterior cingulate cortex in obsessive-compulsive disorder. Cortex doi:10.1016/j.cortex.2012.09.001

  • Latora V, Marchiori M (2001a) Efficient behavior of small-world networks. Phys Rev Lett 87(19):198701

    Article  CAS  PubMed  Google Scholar 

  • Latora V, Marchiori M (2001b) Efficient behavior of small-world networks. Phys Rev Lett 87:198701

    Article  CAS  PubMed  Google Scholar 

  • Mataix-Cols D, Wooderson S, Lawrence N, Brammer MJ, Speckens A, Phillips ML (2004) Distinct neural correlates of washing, checking, and hoarding symptom dimensions in obsessive-compulsive disorder. Arch Gen Psychiatry 61:564–576

    Article  PubMed  Google Scholar 

  • Menzies L, Achard S, Chamberlain SR, Fineberg N, Chen CH, del Campo N, Sahakian BJ, Robbins TW, Bullmore E (2007) Neurocognitive endophenotypes of obsessive-compulsive disorder. Brain 130:3223–3236

    Article  PubMed  Google Scholar 

  • Menzies L, Williams GB, Chamberlain SR, Ooi C, Fineberg N, Suckling J, Sahakian BJ, Robbins TW, Bullmore ET (2008) White matter abnormalities in patients with obsessive-compulsive disorder and their first-degree relatives. Am J Psychiatry 165:1308–1315

    Article  PubMed  Google Scholar 

  • Nestadt G, Samuels J, Riddle M, Bienvenu OJ 3rd, Liang KY, LaBuda M, Walkup J, Grados M, Hoehn-Saric R (2000) A family study of obsessive-compulsive disorder. Arch Gen Psychiatry 57:358–363

    Article  CAS  PubMed  Google Scholar 

  • Newman ME (2006) Modularity and community structure in networks. Proc Natl Acad Sci USA 103:8577–8582

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Newman MEJ, Girvan M (2004) Finding and evaluating community structure in networks. Phys Rev E 69:026113

    Article  CAS  Google Scholar 

  • Niendam TA, Laird AR, Ray KL, Dean YM, Glahn DC, Carter CS (2012) Meta-analytic evidence for a superordinate cognitive control network subserving diverse executive functions. Cogn Affect Behav Neurosci 12:241–268

    Article  PubMed Central  PubMed  Google Scholar 

  • Pauls DL, Alsobrook JP 2nd, Goodman W, Rasmussen S, Leckman JF (1995) A family study of obsessive-compulsive disorder. Am J Psychiatry 152:76–84

    CAS  PubMed  Google Scholar 

  • Peng ZW, Yang WH, Miao GD, Jing J, Chan RC (2011) The Chinese version of the Obsessive-Compulsive Inventory-Revised Scale: replication and extension to non-clinical and clinical individuals with OCD symptoms. BMC Psychiatry 11:129

    Article  PubMed Central  PubMed  Google Scholar 

  • Pujol J, Soriano-Mas C, Alonso P, Cardoner N, Menchon JM, Deus J, Vallejo J (2004) Mapping structural brain alterations in obsessive-compulsive disorder. Arch Gen Psychiatry 61:720–730

    Article  PubMed  Google Scholar 

  • Radua J, Mataix-Cols D (2009) Voxel-wise meta-analysis of grey matter changes in obsessive-compulsive disorder. Br J Psychiatry 195:393–402

    Article  PubMed  Google Scholar 

  • Redies C, Puelles L (2001) Modularity in vertebrate brain development and evolution. BioEssays 23:1100–1111

    Article  CAS  PubMed  Google Scholar 

  • Reichardt J, Bornholdt S (2006) When are networks truly modular? Physica D 224:20–26

    Article  Google Scholar 

  • Rotge JY, Guehl D, Dilharreguy B, Tignol J, Bioulac B, Allard M, Burbaud P, Aouizerate B (2009) Meta-analysis of brain volume changes in obsessive-compulsive disorder. Biol Psychiatry 65:75–83

    Article  PubMed  Google Scholar 

  • Seeley WW, Crawford RK, Zhou J, Miller BL, Greicius MD (2009) Neurodegenerative diseases target large-scale human brain networks. Neuron 62:42–52

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Shin YW, Yoo SY, Lee JK, Ha TH, Lee KJ, Lee JM, Kim IY, Kim SI, Kwon JS (2007) Cortical thinning in obsessive compulsive disorder. Hum Brain Mapp 28:1128–1135

    Article  PubMed  Google Scholar 

  • Spielberger DC (1983) Manual for the State-Trait Anxiety Inventory (STAI). Consulting Psychologists Press, Palo Alto

    Google Scholar 

  • Sporns O, Chialvo DR, Kaiser M, Hilgetag CC (2004) Organization, development and function of complex brain networks. Trends Cogn Sci 8:418–425

    Article  PubMed  Google Scholar 

  • Spreen O, Strauss E (1991) A compendium of neuropsychological tests: Administration, norms, and commentary. Oxford University Press, New York

    Google Scholar 

  • Strogatz SH (2001) Exploring complex networks. Nature 410:268–276

    Article  CAS  PubMed  Google Scholar 

  • Viard A, Flament MF, Artiges E, Dehaene S, Naccache L, Cohen D, Mazet P, Mouren MC, Martinot JL (2005) Cognitive control in childhood-onset obsessive-compulsive disorder: a functional MRI study. Psychol Med 35:1007–1017

    Article  PubMed  Google Scholar 

  • Watts DJ, Strogatz SH (1998) Collective dynamics of ‘small-world’ networks. Nature 393:440–442

    Article  CAS  PubMed  Google Scholar 

  • Whiteside SP, Port JD, Abramowitz JS (2004) A meta-analysis of functional neuroimaging in obsessive-compulsive disorder. Psychiatry Res 132:69–79

    Article  PubMed  Google Scholar 

  • Wu K, Taki Y, Sato K, Kinomura S, Goto R, Okada K, Kawashima R, He Y, Evans AC, Fukuda H (2012) Age-related changes in topological organization of structural brain networks in healthy individuals. Hum Brain Mapp 33:552–568

    Article  CAS  PubMed  Google Scholar 

  • Zhang T, Wang J, Yang Y, Wu Q, Li B, Chen L, Yue Q, Tang H, Yan C, Lui S, Huang X, Chan RC, Zang Y, He Y, Gong Q (2011) Abnormal small-world architecture of top-down control networks in obsessive-compulsive disorder. J Psychiatry Neurosci 36:23–31

    Article  PubMed Central  PubMed  Google Scholar 

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Acknowledgments

This study was partly supported by National Institutes of Health (EB006733, EB008374, EB009634, AG041721), the National Science Fund China Young Investigator Award (81088001), the National Key Technologies R&D Program (2012BAI36B01), National Natural Science Foundation of China (81201049), The Knowledge Innovation Project of the Chinese Academy of Sciences (KSCX2-EW-J-8), and also by a grant from the initiation fund of the CAS/SAFEA International Partnership Programme for Creative Research Teams to Raymond Chan.

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The authors declare no conflict of interest.

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Authors and Affiliations

  1. Department of Radiology and BRIC, University of North Carolina, 130 Mason Farm Road, Chapel Hill, NC, 27599-7513, USA

    Ziwen Peng, Feng Shi & Dinggang Shen

  2. Department of Psychology, South China Normal University, Guangzhou, China

    Ziwen Peng

  3. Medical Imaging Center, The First Affiliated Hospital of Jinan University, Guangzhou, China

    Changzheng Shi

  4. Guangzhou Psychiatry Hospital, Guangzhou, China

    Qiong Yang

  5. Neuropsychology and Applied Cognitive Neuroscience Laboratory, Key Laboratory of Mental Health, Institute of Psychology, Chinese Academy of Sciences, Beijing, China

    Raymond C. K. Chan

  6. Department of Brain and Cognitive Engineering, Korea University, Seoul, Korea

    Dinggang Shen

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  1. Ziwen Peng
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Correspondence to Dinggang Shen.

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Peng, Z., Shi, F., Shi, C. et al. Disrupted cortical network as a vulnerability marker for obsessive–compulsive disorder. Brain Struct Funct 219, 1801–1812 (2014). https://doi.org/10.1007/s00429-013-0602-y

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  • DOI: https://doi.org/10.1007/s00429-013-0602-y

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